(Stroke. 1996;27:1342-1346.)
© 1996 American Heart Association, Inc.
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the Department of Neurosurgery, Hokkaido University School of Medicine, Sapporo, Japan.
| Abstract |
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Methods We analyzed 35 patients with adult moyamoya disease (patient age, over 20 years), 24 patients with initial onset of intracerebral hemorrhage, and 11 patients with initial onset of cerebral ischemia who underwent both direct bypass surgery of the superficial temporal artery to the middle cerebral artery anastomosis and indirect revascularization of encephalo-duro-arterio-myo-synangiosis.
Results Of 24 patients with hemorrhagic-type disease, 3 showed rebleeding; of 11 patients with the ischemic type, 2 showed intracerebral hemorrhage after surgery. Overall, 5 of 35 patients (14.3%) had hemorrhage after revascularization surgery (mean follow-up period, 6.4 years). Postoperative angiography revealed that direct anastomosis is effective whereas indirect revascularization is not always effective for adult moyamoya disease. Moyamoya vessels, which are supposed to be responsible for hemorrhage, decreased in 25% of patients.
Conclusions Revascularization surgery cannot always prevent rebleeding. However, a decrease in moyamoya vessels was induced by surgery, which may reduce the risk of hemorrhage more effectively than conservative treatment. In cases of adult moyamoya disease, direct bypass is particularly important, since the indirect revascularization is not as useful in adult cases as in pediatric cases.
Key Words: cerebral hemorrhage moyamoya disease extracranial-intracranial arterial bypass
| Introduction |
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In this study, we analyzed 35 consecutive patients with adult moyamoya disease who underwent combined surgical therapy by both direct revascularization and indirect revascularization. In particular, the following two points were analyzed: (1) Can this combined surgical revascularization surgery prevent rebleeding in the hemorrhagic type of adult moyamoya disease? (2) Does indirect or direct bypass provide more effective revascularization for the brain in adult moyamoya cases?
| Subjects and Methods |
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Angiographic Analysis
As previously shown, MR angiography is becoming a reliable diagnostic modality for moyamoya disease.12 However, in this study, all patients underwent complete conventional angiography before and after surgery because precise analysis of angiographic findings was necessary, especially to demonstrate the changes in moyamoya vessels. Angiography was performed 6 months after surgery in most cases. Postoperative evaluations of the effectiveness of direct and indirect bypass were made as follows: (1) Direct anastomosis (STA-MCA) was evaluated as "good" when the width of the anastomosed STA increased and the site of anastomosis was clearly identified. In other words, direct bypass was evaluated as "poor" if these criteria were not met. (2) Indirect bypass (EDAMS) was evaluated as good when the middle meningeal artery, STA, and deep temporal artery (muscle branch) made fine new channels to the cortical artery. Otherwise, this revascularization was evaluated as poor. The changes in moyamoya vessels were also evaluated by simple comparison between the preoperative and postoperative angiography.
| Results |
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The mean interval between the first and second hemorrhage was 4.8 years after surgical therapy. Fortunately, none of the patients died even after recurrent hemorrhage, although 1 patient remains in a vegetative state because of the second hemorrhage.
Postoperative Angiographic Change
In the 35 adult cases, 47 sides were completely examined by conventional angiography (including arterial digital subtraction angiography) before and after surgery. For comparison with pediatric moyamoya disease, preoperative and postoperative angiography of 22 sides in pediatric moyamoya patients were also analyzed.
Comparison Between Direct Revascularization by STA-MCA Anastomosis and Indirect Revascularization by EDAMS
The effects in the adult and pediatric groups of each revascularization method are summarized in Table 2
. In adult patients, direct revascularization of STA-MCA was highly effective (90%), whereas indirect revascularization was not very effective. Fig 2
shows representative cases.
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In pediatric moyamoya disease, STA-MCA anastomosis was effective in 68% of cases, which was significantly lower than that in adult moyamoya disease. However, indirect revascularization by EDAMS was effective in 100% without any exception. Statistical analysis revealed that direct bypass is more effective in adult cases than pediatric cases (P<.05,
2 test) and that indirect revascularization is more effective in pediatric cases than adult cases (P<.001,
2 test). Fig 3
shows representative cases of adult and pediatric moyamoya disease, revealing good STA-MCA anastomosis and poor EDAMS in adult cases and good EDAMS in pediatric cases.
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Change in Moyamoya Vessels After Surgery
In adult cases, moyamoya vessels diminished in only 25%, whereas there was no significant change in moyamoya vessels in 75%. However, in pediatric cases, significant change in moyamoya vessels was seen in 100%. There is a significant difference in the diminishment of moyamoya vessels between pediatric and adult cases (P<.001,
2 test). Fig 4
shows representative cases, revealing no significant change in moyamoya vessels in an adult patient and reduction in moyamoya vessel after surgery in a pediatric patient.
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| Discussion |
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There is controversy regarding the effect of this revascularization surgery in preventing the recurrent ICH seen in adult moyamoya disease.8 9 10 18 19 In discussion of this controversial issue, the mechanism of intracerebral bleeding seen in moyamoya disease must be considered. Presently, the associated small aneurysm in the circle of Willis (mainly the posterior circulation) and microaneurysm of the abnormally dilated moyamoya vessels are considered the origins of hemorrhage.20 21 22 23 When aneurysms are detected in the circle of Willis or in moyamoya vessels on angiography, these aneurysms should be treated. Indeed, Hamada et al22 reported two cases of moyamoya disease with repeated intraventricular hemorrhage due to microaneurysm rupture and the clipping or trapping of parent arteries. Recently, endovascular treatment for the saccular aneurysm in moyamoya disease using electrically detachable coil was also reported.23 However, in general, it is unusual for these small microaneurysms to be detected on angiography, especially in cases involving the hemorrhagic type of moyamoya disease, as in hypertensive intracerebral hematoma. However, these microaneurysms are supposed to be induced by hemodynamic stress to the moyamoya vessels, which are abnormally dilated to compensate for ischemia due to steno-occlusive change in the main trunk of the anterior circulation of the circle of Willis.13 22 24 Therefore, practical management for the hemorrhagic-type moyamoya disease, in which apparent microaneurysms responsible for hemorrhage are not demonstrated on angiography, is to decrease this hemodynamic stress and consequently induce a decrease in the moyamoya vessels. The rationale for revascularization surgery to reduce the risk of hemorrhage in moyamoya disease is deduced from the concept that the appropriate revascularization can decrease hemodynamic stress on the collateral circulation.9 10
There has not been any randomized study to test the practical effect of this revascularization surgery on reducing the risk of hemorrhage in moyamoya disease. The clinical course of conservative therapy for the adult hemorrhagic type of moyamoya disease has not been discussed thoroughly.8 25 A nationwide survey in Japan by Kudo and Fukuda2 in 1979 showed that 10 of 58 patients (17%) whose age at onset was more than 16 years had recurrent hemorrhage. Another survey by Nishimoto et al26 also revealed that 33% of 175 patients with hemorrhagic attacks due to moyamoya disease sought medical attention because of repeated bleeding. The incidence of rebleeding in adult moyamoya disease reported in that study seems to be higher than the incidence in our study (14.5%). Wanifuchi et al27 reported 59 cases of adult moyamoya disease, which included 38 patients treated conservatively and 21 treated with surgical therapy. In their article, they concluded that hemorrhage recurrence in the surgical group was much less common than in the conservative-treatment group. These results suggest that surgical treatment is superior to conservative therapy in reducing the risk of rebleeding. Moreover, our results clearly revealed that decrease of moyamoya vessels was induced by revascularization surgery even in adult cases, although the effect is less than that in pediatric cases. However, these data are not well randomized, and further long-term follow-up study and discrete analysis are required to establish the superiority of surgery. In addition, long-term follow-up of pediatric moyamoya patients who were surgically treated is tremendously important to evaluate the long-term results of revascularization surgery.9 10
Our results also disclosed a very important aspect of surgical therapy for adult moyamoya disease: direct revascularization by STA-MCA is much more effective than indirect revascularization in adult moyamoya disease.28 However, in pediatric moyamoya disease, indirect revascularization is 100% effective, whereas direct revascularization has failed in some cases because of the extraordinarily small donor and recipient vessels. The reason why indirect revascularization was not as effective in adult cases is not clear. However, the severity of cerebral ischemia in adult patients, which is considered the main driving force that induces the neovascularization from indirect revascularization, is mild. Moreover, as we have shown, basic fibroblast growth factor in the cerebrospinal fluid, a cytokine which we consider important in inducing neovascularization in moyamoya disease, is not as elevated in adult compared with pediatric patients.29
In conclusion, the superiority of surgical treatment for the adult hemorrhagic type of moyamoya disease must be tested by long-term follow-up study. However, as we have shown, effective revascularization surgery with both direct and indirect revascularization can decrease the moyamoya vessels in adult patients. Direct revascularization by STA-MCA anastomosis is an indispensable method for effective revascularization, especially in adult patients.
| Selected Abbreviations and Acronyms |
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| Acknowledgments |
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| Footnotes |
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Received March 4, 1996; revision received April 9, 1996; accepted April 9, 1996.
| References |
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